cis-Prenyltransferase AtCPT6 produces a family of very short-chain polyisoprenoids in planta

Surmacz, Liliana; Płochocka, Danuta; Kania, Magdalena; Danikiewicz, Witold; Świeżewska, Ewa

doi:10.1016/j.bbalip.2013.11.011

Cited by 32 publications

(38 citation statements)

References 43 publications

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“…AtCPT1 and AtCPT6 are expressed exclusively in root tissue, localize to the endomembrane system, and synthesize long-chain (C95-110) and short-chain (C35) polyprenols, respectively (Cunillera et al, 2000;Oh et al, 2000;Kera et al, 2012;Surmacz et al, 2014). The physiological function(s) of these polyprenols are still unclear.…”

Section: Discussionmentioning

confidence: 99%

Polyprenols Are Synthesized by a Plastidial cis-Prenyltransferase and Influence Photosynthetic Performance

et al. 2017

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Plants accumulate a family of hydrophobic polymers known as polyprenols, yet how they are synthesized, where they reside in the cell, and what role they serve is largely unknown. Using Arabidopsis thaliana as a model, we present evidence for the involvement of a plastidial cis-prenyltransferase (AtCPT7) in polyprenol synthesis. Gene inactivation and RNAi-mediated knockdown of AtCPT7 eliminated leaf polyprenols, while its overexpression increased their content. Complementation tests in the polyprenol-deficient yeast Δrer2 mutant and enzyme assays with recombinant AtCPT7 confirmed that the enzyme synthesizes polyprenols of ;55 carbons in length using geranylgeranyl diphosphate (GGPP) and isopentenyl diphosphate as substrates. Immunodetection and in vivo localization of AtCPT7 fluorescent protein fusions showed that AtCPT7 resides in the stroma of mesophyll chloroplasts. The enzymatic products of AtCPT7 accumulate in thylakoid membranes, and in their absence, thylakoids adopt an increasingly "fluid membrane" state. Chlorophyll fluorescence measurements from the leaves of polyprenol-deficient plants revealed impaired photosystem II operating efficiency, and their thylakoids exhibited a decreased rate of electron transport. These results establish that (1) plastidial AtCPT7 extends the length of GGPP to ;55 carbons, which then accumulate in thylakoid membranes; and (2) these polyprenols influence photosynthetic performance through their modulation of thylakoid membrane dynamics.

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Section: Discussionmentioning

confidence: 99%

Polyprenols Are Synthesized by a Plastidial cis-Prenyltransferase and Influence Photosynthetic Performance

et al. 2017

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“…N-Glycans are crucial for plant growth under stress conditions (Strasser, 2016); therefore, reprogramming of the Dol-14 to Dol-17 biosynthetic route could be indispensable for plant homeostasis. Long-and short-chain Dols are possibly not involved in protein glycosylation (Schenk et al, 2001;Surmacz et al, 2014) but instead could act as a shield against ROS or fulfill other as yet unknown functions.…”

Section: Discussionmentioning

confidence: 99%

“…The changing ratio of Dol families and the contrasting responses of different CPT genes in response to osmotic stress suggested that at least three CPTs take part in Dol biosynthesis. Since CPT6 produces shorter prenyl alcohols (Kera et al, 2012;Surmacz et al, 2014), CPT3 and/or CPT7 might operate to synthesize dominating Dols. Moreover, out of six CPTs expressed in Arabidopsis roots, CPT3 seems the most similar to the yeast Rer2 CPT, synthesizing a family of Dols with Dol-16 dominating ( Fig.…”

Section: Dol Metabolism Upon Osmotic Stress: Biochemical Analysismentioning

confidence: 99%

Modeling of Dolichol Mass Spectra Isotopic Envelopes as a Tool to Monitor Isoprenoid Biosynthesis

et al. 2017

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The cooperation of the mevalonate (MVA) and methylerythritol phosphate (MEP) pathways, operating in parallel in plants to generate isoprenoid precursors, has been studied extensively. Elucidation of the isoprenoid metabolic pathways is indispensable for the rational design of plant and microbial systems for the production of industrially valuable terpenoids. Here, we describe a new method, based on numerical modeling of mass spectra of metabolically labeled dolichols (Dols), designed to quantitatively follow the cooperation of MVA and MEP reprogrammed upon osmotic stress (sorbitol treatment) in Arabidopsis (Arabidopsis thaliana). The contribution of the MEP pathway increased significantly (reaching 100%) exclusively for the dominating Dols, while for long-chain Dols, the relative input of the MEP and MVA pathways remained unchanged, suggesting divergent sites of synthesis for dominating and long-chain Dols. The analysis of numerically modeled Dol mass spectra is a novel method to follow modulation of the concomitant activity of isoprenoid-generating pathways in plant cells; additionally, it suggests an exchange of isoprenoid intermediates between plastids and peroxisomes.Isopentenyl diphosphate (IPP), the building block of isoprenoids, the most numerous class of secondary metabolites, is derived in plants from two pathways operating in parallel: the cytoplasmic mevalonate (MVA) and the plastidic methylerythritol phosphate (MEP) pathways (Rohmer, 1999;Pulido et al., 2012).Analysis of over 130 isoprenoids has shown that, in angiosperms under standard growth conditions, carotenoids and chlorophyll phytyl chains on the one hand and phytosterols on the other are made nearly exclusively via a single pathway (MEP and MVA, respectively), while numerous other isoprenoids, including dolichols (Dols; Skorupinska-Tudek et al., 2008), are of mixed origin (Hemmerlin et al., 2012).The cooperation of the two pathways (often called cross talk) is considered essential for plant adaptive responses to biotic and abiotic stresses. Consequently, their relative contributions to the formation of IPP are modulated, and the expression of particular genes of the MVA and MEP pathways is frequently correlated with stress (pathogen attack, elicitation, wounding, etc.;Hemmerlin et al., 2012) or plant development (Opitz et al., 2014). Interestingly, the effect of stress on the regulation of the MEP-MVA balance has so far been analyzed only qualitatively.Several methodologies have been employed to unravel the relative contributions of the MVA and MEP pathways to isoprenoids, such as metabolic labeling with isotopically labeled precursors (stable isotopes or radioisotopes were used), followed by structural analysis of the product of interest or blockage of the pathway (chemical, with pathway-specific inhibitors, or genetic), followed by quantification of the isoprenoid intermediates and/or end products. The advantages

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“…Z,E-DecPP from M. tuberculosis was the first described cis-PT utilizing a different allylic substrate other than FPP (17,31). In Arabidopsis thaliana, AtCPT6 functions in response to abiotic stress (32,33); however, the AtCPT6 product most likely does not serve as lipid carrier in glycosylation reactions.…”

Section: Classification Of Cis-ptsmentioning

confidence: 99%

cis-Prenyltransferase: New Insights into Protein Glycosylation, Rubber Synthesis, and Human Diseases

Grabińska

Park

Sessa

2016

Journal of Biological Chemistry

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cis-Prenyltransferases (cis-PTs) constitute a large family of enzymes conserved during evolution and present in all domains of life. cis-PTs catalyze consecutive condensation reactions of allylic diphosphate acceptor with isopentenyl diphosphate (IPP) in the cis (Z) configuration to generate linear polyprenyl diphosphate. The chain lengths of isoprenoid carbon skeletons vary widely from neryl pyrophosphate (C 10 ) to natural rubber (C >10,000 ). The homo-dimeric bacterial enzyme, undecaprenyl diphosphate synthase (UPPS), has been structurally and mechanistically characterized in great detail and serves as a model for understanding the mode of action of eukaryotic cis-PTs. However, recent experiments have revealed that mammals, fungal, and long-chain plant cis-PTs are heteromeric enzymes composed of two distantly related subunits. In this review, the classification, function, and evolution of cis-PTs will be discussed with a special emphasis on the role of the newly described NgBR/Nus1 subunit and its plants' orthologs as essential, structural components of the cis-PTs activity.

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cis-Prenyltransferase AtCPT6 produces a family of very short-chain polyisoprenoids in planta

Cited by 32 publications

References 43 publications

Polyprenols Are Synthesized by a Plastidial cis-Prenyltransferase and Influence Photosynthetic Performance

Polyprenols Are Synthesized by a Plastidial cis-Prenyltransferase and Influence Photosynthetic Performance

Modeling of Dolichol Mass Spectra Isotopic Envelopes as a Tool to Monitor Isoprenoid Biosynthesis

cis-Prenyltransferase: New Insights into Protein Glycosylation, Rubber Synthesis, and Human Diseases

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